Short-Term Activity Cycles Impede Information Transmission in Ant Colonies
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RESEARCH ARTICLE Short-term activity cycles impede information transmission in ant colonies Thomas O. Richardson1*, Jonas I. Liechti2☯, Nathalie Stroeymeyt1☯, Sebastian Bonhoeffer2, Laurent Keller1 1 Department of Ecology and Evolution, University of Lausanne, Switzerland, 2 Department of Environmental Systems Science, ETH ZuÈrich, Switzerland ☯ These authors contributed equally to this work. * [email protected], [email protected] a1111111111 a1111111111 a1111111111 a1111111111 Abstract a1111111111 Rhythmical activity patterns are ubiquitous in nature. We study an oscillatory biological sys- tem: collective activity cycles in ant colonies. Ant colonies have become model systems for research on biological networks because the interactions between the component parts are visible to the naked eye, and because the time-ordered contact network formed by these OPEN ACCESS interactions serves as the substrate for the distribution of information and other resources Citation: Richardson TO, Liechti JI, Stroeymeyt N, throughout the colony. To understand how the collective activity cycles influence the contact Bonhoeffer S, Keller L (2017) Short-term activity network transport properties, we used an automated tracking system to record the move- cycles impede information transmission in ant colonies. PLoS Comput Biol 13(5): e1005527. ment of all the individuals within nine different ant colonies. From these trajectories we https://doi.org/10.1371/journal.pcbi.1005527 extracted over two million ant-to-ant interactions. Time-series analysis of the temporal fluc- Editor: Joseph Ayers, Northeastern University, tuations of the overall colony interaction and movement rates revealed that both the period UNITED STATES and amplitude of the activity cycles exhibit a diurnal cycle, in which daytime cycles are faster Received: September 7, 2016 and of greater amplitude than night cycles. Using epidemiology-derived models of transmis- sion over networks, we compared the transmission properties of the observed periodic con- Accepted: April 20, 2017 tact networks with those of synthetic aperiodic networks. These simulations revealed that Published: May 10, 2017 contrary to some predictions, regularly-oscillating contact networks should impede informa- Copyright: © 2017 Richardson et al. This is an tion transmission. Further, we provide a mechanistic explanation for this effect, and present open access article distributed under the terms of evidence in support of it. the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are available Author summary from the Dryad Digital Repository: http://dx.doi. org/10.5061/dryad.65q64. Many complex biological systems, from cardiac tissues to entire animal populations, exhibit rhythmical oscillations. Here we studied a textbook example of a complex living Funding: TOR acknowledges an EU Marie Curie system±colonies of ants, which exhibit short (15 minute) collective activity Actions Fellowship (`Mapping spatial interaction Leptothorax networks in honeybee colonies', no. 30114). LK cycles. In ant colonies, information, food, and chemical signals are transported through- acknowledges funding by the European Research out the group via worker-to-worker physical contacts, and it has therefore been suggested Council (ERC Advanced Grant, `Social Life', no. that the activity cycles might serve to increase the rapidity of information transmission. 249375), and Swiss National Science Foundation To test this, we used an automatic ant tracking system to identify physical contacts (`The determinants of social organisation in ants', between workers, from which we reconstructed the dynamical network of physical con- no. 310030B\textunderscore 133121). The funders had no role in study design, data collection and tacts. We used models of information transmission derived from the study of contagious PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1005527 May 10, 2017 1 / 17 Activity cycles and information transmission in ant colonies analysis, decision to publish, or preparation of the manuscript. diseases to simulate information transmission over the rhythmical contact networks, Competing interests: The authors have declared which we compared against a set of comparable networks that exhibited no rhythms. that no competing interests exist. These comparisons showed that, contrary to the expectations, oscillatory activity cycles slowed down information transmission rather than speeding it up. We suggest that the colony activity cycles might serve to ensure that old or out-of-date information is quickly expunged, and potentially reduce interference between different information streams. Introduction Cyclical activity patterns are found at every level of biological organization, from genes to cells, organs, and societies, and span many orders of magnitude in space and time. For instance, cyclical activity is found at the smallest spatial scale in the regulation of circadian Clock genes [1], and at the largest, in the cyclical fluctuation of populations of predators and prey [2, 3]. Similarly, cyclical phenomena occur at frequencies ranging from roughly once per second for the firing patterns of human cardiac pacemaker cells [4], to once every 13 or 17 years for reproductive cycles in cicadas [5]. Although cyclical activity patterns can be driven by an exogenous signal, such as diurnal, lunar and seasonal cycles, there are also many systems in which cyclical activity emerges in the absence of a pacemaker. For example, in humans an applauding audience may spontaneously break into bouts of synchronized clapping [6]. Similarly, the synchronization (or anti-synchro- nization) of courting fireflies [7] and calling in frog choruses [8] is an emergent property, though these are so regular that it was originally hypothesized that there must exist a leader that sets the rhythm [9, 10]. In this paper we study short-term activity cycles (henceforth, STACs) in colonies of the ant Leptothorax acervorum (Fig 1a). These ants display a remarkable degree of synchronization in their activity patterns, resulting in quasi-periodic oscillations in the overall rate of physical contacts between nestmates (S1 Video), with roughly three to four peaks per hour [11, 12, 13]. In colonies of social insectsÐants, bees, wasps & termitesÐlife within the nest is dominated by frequent physical contact between nestmates, such as allogrooming, and oral fluid exchange. This contact-based `infrastructure' serves as a decentralized communication network for the transport of a wide variety of information-bearing materials. These include complex mixtures of cuticular hydrocarbons that are crucial for nestmate-recognition [14, 15, 16] and task-allo- cation [17], chemical fertility-signals advertising the presence of the queen [18, 19, 20], and growth hormones controlling the development of the brood [21]. Furthermore, the contacts themselves can convey information, without chemical transfer. For example, information transmission during cooperative foraging involves both ritualized tactile motor displays [22, 23, 24], and also purely passive (i.e. kinetic) encounters [25]. Given that physical contacts pro- vide a substrate for communication, it follows that the speed of information transfer should depend upon the contact rate. Indeed, [26] first predicted that when activity is synchronized, information should spread more rapidly (see also [11, 13]). Although there are many examples of complex networksÐboth naturally-occurring, and human designedÐthat function to enhance transmission of information and other resources [27, 28], there are also examples in which the network structure functions to impede transmission of harmful materials such as pathogens [29] or poisons [30]. Therefore, in what follows we use a combination of experiment and simulation modelling to test if and how STACs influence transmission in ant colonies. To test whether STACs could potentially influence information transmission, we used an automated tracking system [31] in which a unique barcode tag is attached to the thorax of PLOS Computational Biology | https://doi.org/10.1371/journal.pcbi.1005527 May 10, 2017 2 / 17 Activity cycles and information transmission in ant colonies Fig 1. Short-term activity cycles. (a)Leptothorax acervorum workers with unique ARtag markers glued to the thorax. The inset illustrates the geometrical approximation used to infer ant-to-ant contacts. Blue trapezoid: A head-to-head contact with the grey ant is detected as the angle between them is high (θ120Ê), and the interaction point (yellow circle) of the blue ant enters into the trapezoid of the grey. Green trapezoid: When the angular difference threshold is relaxed (θ60Ê), both head-to-body and head-to-head contacts are detected. Red trapezoid: No contact is detected as the ants are too far apart. (b) Image of the nest during a period of high activity (colony 13, replicate 1, 12:34 p.m., indicated by the vertical line in panel e). The triangle indicates the entrance. The axis tick-marks denote 1cm units. Panels c-d summarise the spatial distribution of the activity occurring during 1 minute preceding the midday activity peak (12:33±12:34 p.m.). (c) Ant spatial trajectories. Each ant is arbitrarily assigned a different colour. (d) Contacts between ants. Black lines indicate contacts between ants. Colours correspond to those in panel c. Panels